A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson's disease.
Journal
PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
received:
20
04
2022
accepted:
27
10
2022
revised:
01
12
2022
pubmed:
18
11
2022
medline:
6
12
2022
entrez:
17
11
2022
Statut:
epublish
Résumé
Surviving in an uncertain environment requires not only the ability to select the best action, but also the flexibility to withhold inappropriate actions when the environmental conditions change. Although selecting and withholding actions have been extensively studied in both human and animals, there is still lack of consensus on the mechanism underlying these action regulation functions, and more importantly, how they inter-relate. A critical gap impeding progress is the lack of a computational theory that will integrate the mechanisms of action regulation into a unified framework. The current study aims to advance our understanding by developing a neurodynamical computational theory that models the mechanism of action regulation that involves suppressing responses, and predicts how disruption of this mechanism can lead to motor deficits in Parkinson's disease (PD) patients. We tested the model predictions in neurotypical individuals and PD patients in three behavioral tasks that involve free action selection between two opposed directions, action selection in the presence of conflicting information and abandoning an ongoing action when a stop signal is presented. Our results and theory suggest an integrated mechanism of action regulation that affects both action initiation and inhibition. When this mechanism is disrupted, motor behavior is affected, leading to longer reaction times and higher error rates in action inhibition.
Identifiants
pubmed: 36395336
doi: 10.1371/journal.pcbi.1010111
pii: PCOMPBIOL-D-22-00614
pmc: PMC9714880
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1010111Subventions
Organisme : NINDS NIH HHS
ID : U01 NS098961
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS097782
Pays : United States
Informations de copyright
Copyright: © 2022 Zhong et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Trends Cogn Sci. 2004 Apr;8(4):170-7
pubmed: 15050513
Trends Cogn Sci. 2008 Nov;12(11):418-24
pubmed: 18799345
J Neurosci. 2015 Jan 14;35(2):786-94
pubmed: 25589771
Neuron. 2009 Sep 10;63(5):568-83
pubmed: 19755101
PLoS Comput Biol. 2021 Oct 1;17(10):e1009429
pubmed: 34597294
Nat Neurosci. 2011 Sep 25;14(11):1462-7
pubmed: 21946325
Curr Biol. 2016 Apr 4;26(7):916-20
pubmed: 26996501
Cognition. 2010 Aug;116(2):168-76
pubmed: 20471007
Psychol Rev. 2014 Jan;121(1):66-95
pubmed: 24490789
Nature. 1997 Mar 13;386(6621):167-70
pubmed: 9062187
Child Neuropsychol. 2006 Apr;12(2):125-40
pubmed: 16754533
Brain. 1981 Mar;104(Pt 1):167-86
pubmed: 7470841
PLoS Comput Biol. 2015 Mar 30;11(3):e1004171
pubmed: 25821964
Front Neurosci. 2014 Jan 22;7:276
pubmed: 24478620
J Neurophysiol. 2003 May;89(5):2577-90
pubmed: 12611995
PLoS Comput Biol. 2015 Sep 22;11(9):e1004402
pubmed: 26394299
Psychol Med. 2010 Feb;40(2):263-72
pubmed: 19573261
Cereb Cortex. 2007 Dec;17(12):2972-9
pubmed: 17389629
Neural Comput. 2005 May;17(5):1084-108
pubmed: 15829101
Mov Disord. 2011 Aug 1;26(9):1657-62
pubmed: 21542021
Annu Rev Neurosci. 2010;33:269-98
pubmed: 20345247
Mov Disord. 2015 Mar;30(3):328-38
pubmed: 25688872
Percept Psychophys. 1979 Apr;25(4):249-63
pubmed: 461085
J Exp Psychol Hum Percept Perform. 2009 Jun;35(3):835-54
pubmed: 19485695
Elife. 2021 Sep 06;10:
pubmed: 34486520
Neuroimage. 2010 Apr 15;50(3):1313-9
pubmed: 20056157
Trends Cogn Sci. 2010 Jan;14(1):31-9
pubmed: 20005767
Nat Commun. 2017 Mar 03;8:14624
pubmed: 28256513
World J Methodol. 2014 Sep 26;4(3):133-43
pubmed: 25332912
Nat Neurosci. 2003 Feb;6(2):115-6
pubmed: 12536210
Front Aging Neurosci. 2018 Oct 23;10:331
pubmed: 30405399
J Neurophysiol. 2012 Dec;108(11):2912-30
pubmed: 22993260
Perception. 1985;14(4):471-97
pubmed: 3834388
Nat Neurosci. 2013 Aug;16(8):1118-24
pubmed: 23852117
Exp Psychol. 2010;57(2):149-59
pubmed: 20178958
Psychopharmacology (Berl). 2007 Apr;191(3):461-82
pubmed: 17225164
Nat Neurosci. 2016 Feb;19(2):320-6
pubmed: 26752159
Philos Trans R Soc Lond B Biol Sci. 2007 Sep 29;362(1485):1585-99
pubmed: 17428779
Brain Cogn. 2004 Nov;56(2):234-52
pubmed: 15518938
Cortex. 2016 Nov;84:111-123
pubmed: 27745848
J Neurol Neurosurg Psychiatry. 2004 Apr;75(4):539-44
pubmed: 15026491
Cogn Affect Behav Neurosci. 2016 Oct;16(5):825-35
pubmed: 27160368
Front Neuroeng. 2012 Apr 04;5:5
pubmed: 22493577
J Neurol. 2015 Jun;262(6):1541-7
pubmed: 25929662
Nat Commun. 2016 Apr 18;7:11195
pubmed: 27088156
Behav Brain Res. 2002 Dec 2;137(1-2):3-25
pubmed: 12445713
Front Hum Neurosci. 2014 Jun 11;8:419
pubmed: 24966828
Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13852-7
pubmed: 21808009
J Neurophysiol. 2016 Dec 1;116(6):2857-2868
pubmed: 27655964
J Neurosci. 2012 Sep 26;32(39):13396-401
pubmed: 23015430
Cortex. 2015 Aug;69:40-6
pubmed: 25967086
Psychol Rev. 2006 Oct;113(4):700-65
pubmed: 17014301
J Neurosci. 2006 Mar 1;26(9):2424-33
pubmed: 16510720
PLoS Comput Biol. 2021 Dec 23;17(12):e1009718
pubmed: 34941863
Brain Res Brain Res Rev. 1995 Jan;20(1):91-127
pubmed: 7711769
Neuropsychologia. 2009 Jan;47(1):145-57
pubmed: 18761363
Cold Spring Harb Perspect Med. 2012 Jun;2(6):a009282
pubmed: 22675667
Sci Rep. 2018 Sep 24;8(1):14265
pubmed: 30250230
Vision Res. 1999;39(25):4200-16
pubmed: 10755158
J Neurosci. 2009 Oct 7;29(40):12675-85
pubmed: 19812342
Dialogues Clin Neurosci. 2004 Sep;6(3):259-80
pubmed: 22033559
J Neurosci. 2011 Jan 12;31(2):742-52
pubmed: 21228183
Neuroimage. 2012 Mar;60(1):271-8
pubmed: 22209815
Neural Netw. 2006 Oct;19(8):1302-14
pubmed: 16949252
Elife. 2019 Apr 29;8:
pubmed: 31033438
J Neurosci. 2009 May 20;29(20):6436-48
pubmed: 19458215
Hum Brain Mapp. 2013 Sep;34(9):2015-24
pubmed: 22359406
J Neurosci. 2007 Jul 4;27(27):7105-16
pubmed: 17611263
Science. 1999 Jul 9;285(5425):257-60
pubmed: 10398603
Ann N Y Acad Sci. 2011 Dec;1239:118-29
pubmed: 22145881
Semin Neurol. 2017 Apr;37(2):109-117
pubmed: 28511251
J Cogn Neurosci. 2006 Mar;18(3):444-55
pubmed: 16513008
Sci Rep. 2017 Sep 15;7(1):11703
pubmed: 28916824
Front Neural Circuits. 2019 Mar 11;13:15
pubmed: 30914925
J Neurosci. 2011 May 11;31(19):7083-8
pubmed: 21562270
PLoS Comput Biol. 2015 Mar 24;11(3):e1004104
pubmed: 25803729
J Exp Psychol Hum Percept Perform. 1988 Aug;14(3):331-44
pubmed: 2971764
Nature. 2006 May 11;441(7090):223-6
pubmed: 16633341
Psychol Rev. 2013 Apr;120(2):329-55
pubmed: 23586447
J Cogn Neurosci. 2010 Jul;22(7):1479-92
pubmed: 19583473
J Neurosci. 1991 May;11(5):1210-23
pubmed: 2027043
J Neurosci. 2007 Apr 4;27(14):3743-52
pubmed: 17409238
Acta Psychol (Amst). 1982 Mar;50(2):179-97
pubmed: 7102359
Nat Rev Neurosci. 2018 Sep;19(9):519-534
pubmed: 30089888
J Neurosci. 2013 Dec 11;33(50):19611-9
pubmed: 24336725
J Neurosci. 2013 Mar 13;33(11):4804-14
pubmed: 23486951
Nat Commun. 2015 Jul 01;6:7428
pubmed: 26130029
J Cogn Neurosci. 2018 Jan;30(1):107-118
pubmed: 28880766
Neuron. 2014 Dec 17;84(6):1329-42
pubmed: 25521381
Neuron. 2005 Mar 3;45(5):801-14
pubmed: 15748854
J Exp Psychol Hum Percept Perform. 1982 Apr;8(2):273-96
pubmed: 6461722
Res Dev Disabil. 2017 Feb;61:1-10
pubmed: 28039814
Front Neurorobot. 2017 Mar 02;11:9
pubmed: 28303100
Psychol Rev. 2007 Apr;114(2):376-97
pubmed: 17500631
Transl Psychiatry. 2014 Sep 09;4:e439
pubmed: 25203170
Neural Netw. 2006 Oct;19(8):1120-36
pubmed: 16945502
J Neurosci. 2006 Jan 4;26(1):186-92
pubmed: 16399686
J Neurosci. 2010 Nov 3;30(44):14657-75
pubmed: 21048123
Science. 1981 Jan 30;211(4481):453-8
pubmed: 7455683